Casein kinase II regulates N-methyl-D-aspartate receptor activity in spinal cords and pain hypersensitivity induced by nerve injury

Journal of Pharmacology and Experimental Therapeutics

Volumn 350, Issue 2, 2014, Pages 301-312

  Chen, Shao Rui ^a   Zhou, Hong Yi ^a   Byun, Hee Sun ^a   Chen, Hong ^a   Pan, Hui Lin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; CASEIN KINASE IIALPHA; CASEIN KINASE IIBETA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; TACROLIMUS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC NEUROPATHY; DORSAL ROOT; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; INTERNEURON; MALE; NERVE CELL; NERVE STIMULATION; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PHARMACOLOGICAL BLOCKING; POSTHERPETIC NEURALGIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD DORSAL HORN; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; TREATMENT RESPONSE;

ANIMALS; CALCINEURIN; CASEIN KINASE II; DIABETIC NEUROPATHIES; HYPERALGESIA; MALE; NEURALGIA; PERIPHERAL NERVE INJURIES; PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD;

EID: 84905013240     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.215855     Document Type: Article

References (61)

1. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, and Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595.
2. Bare DJ, Ghetti B, and Richter JA (1995) The tyrosine kinase inhibitor genistein increases endogenous dopamine release from normal and weaver mutant mouse striatal slices. J Neurochem 65:2096-2104.
3. Blanquet PR (2000) Casein kinase 2 as a potentially important enzyme in the nervous system. Prog Neurobiol 60:211-246.
4. Cai YQ, Chen SR, Han HD, Sood AK, Lopez-Berestein G, and Pan HL (2009) Role of M2, M3, and M4 muscarinic receptor subtypes in the spinal cholinergic control of nociception revealed using siRNA in rats. J Neurochem 111:1000-1010.
5. Campbell JN, Raja SN, Meyer RA, and Mackinnon SE (1988) Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32:89-94.
6. Cervero F and Iggo A (1980) The substantia gelatinosa of the spinal cord: a critical review. Brain 103:717-772.
7. Chaplan SR, Malmberg AB, and Yaksh TL (1997) Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat. J Pharmacol Exp Ther 280:829-838.
8. Charriaut-Marlangue C, Otani S, Creuzet C, Ben-Ari Y, and Loeb J (1991) Rapid activation of hippocampal casein kinase II during long-term potentiation. Proc Natl Acad Sci USA 88:10232-10236.
9. Chen L and Huang LY (1992) Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356:521-523.
10. Chen SR, Hu YM, Chen H, and Pan HL (2014) Calcineurin inhibitor induces pain hypersensitivity by potentiating pre- and postsynaptic NMDA receptor activity in spinal cords. J Physiol 592:215-227.
11. Chen SR and Pan HL (2002) Hypersensitivity of spinothalamic tract neurons associated with diabetic neuropathic pain in rats. J Neurophysiol 87:2726-2733.
12. Chen SR and Pan HL (2005) Effect of systemic and intrathecal gabapentin on allodynia in a new rat model of postherpetic neuralgia. Brain Res 1042:108-113.
13. Chergui K, Svenningsson P, and Greengard P (2005) Physiological role for casein kinase 1 in glutamatergic synaptic transmission. J Neurosci 25:6601-6609.
14. Chung HJ, Huang YH, Lau LF, and Huganir RL (2004) Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. J Neurosci 24:10248-10259.
15. Collini A, De Bartolomeis C, Barni R, Ruggieri G, Bernini M, and Carmellini M (2006) Calcineurin-inhibitor induced pain syndrome after organ transplantation. Kidney Int 70:1367-1370.
16. Correll GE, Maleki J, Gracely EJ, Muir JJ, and Harbut RE (2004) Subanesthetic ketamine infusion therapy: a retrospective analysis of a novel therapeutic approach to complex regional pain syndrome. Pain Med 5:263-275.
17. Devary Y, Gottlieb RA, Smeal T, and Karin M (1992) The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71:1081-1091.
18. Ehlers MD, Zhang S, Bernhadt JP, and Huganir RL (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84:745-755.
19. Fischer G, Mutel V, Trube G, Malherbe P, Kew JN, Mohacsi E, Heitz MP, and Kemp JA (1997) Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 283:1285-1292.
20. Gao X, Kim HK, Chung JM, and Chung K (2005) Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats. Pain 116:62-72.
21. Garver TD, Oyler GA, Harris KA, Polavarapu R, Damuni Z, Lehman RA, and Billingsley ML (1995) Tau phosphorylation in brain slices: pharmacological evidence for convergent effects of protein phosphatases on tau and mitogen-activated protein kinase. Mol Pharmacol 47:745-756.
22. Gracely RH, Lynch SA, and Bennett GJ (1992) Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51:175-194.
23. Grotz WH, Breitenfeldt MK, Braune SW, Allmann KH, Krause TM, Rump JA, and Schollmeyer PJ (2001) Calcineurin-inhibitor induced pain syndrome (CIPS): a severe disabling complication after organ transplantation. Transpl Int 14:16-23.
24. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, and Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695-701.
25. Haystead TA, Sim AT, Carling D, Honnor RC, Tsukitani Y, Cohen P, and Hardie DG (1989) Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337:78-81.
26. Herbert JM, Augereau JM, Gleye J, and Maffrand JP (1990) Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 172: 993-999.
27. Hu YM, Chen SR, Chen H, and Pan HL (2014) Casein kinase II inhibition reverses pain hypersensitivity and potentiated spinal N-methyl-d-aspartate receptor activity caused by calcineurin inhibitor. J Pharmacol Exp Ther 349:239-247.
28. Hua XY, Chen P, and Yaksh TL (1999) Inhibition of spinal protein kinase C reduces nerve injury-induced tactile allodynia in neuropathic rats. Neurosci Lett 276: 99-102.
29. Katsura H, Obata K, Mizushima T, Sakurai J, Kobayashi K, Yamanaka H, Dai Y, Fukuoka T, Sakagami M, and Noguchi K (2006) Activation of Src-family kinases in spinal microglia contributes to mechanical hypersensitivity after nerve injury. J Neurosci 26:8680-8690.
30. Kimura R and Matsuki N (2008) Protein kinase CK2 modulates synaptic plasticity by modification of synaptic NMDA receptors in the hippocampus. J Physiol 586: 3195-3206.
31. Kolaj M, Cerne R, Cheng G, Brickey DA, and Randic M (1994) Alpha subunit of calcium/calmodulin-dependent protein kinase enhances excitatory amino acid and synaptic responses of rat spinal dorsal horn neurons. J Neurophysiol 72: 2525-2531.
32. Krupp JJ, Vissel B, Thomas CG, Heinemann SF, and Westbrook GL (1999) Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+ - dependent inactivation of NMDA receptors. J Neurosci 19:1165-1178.
33. Li DP, Byan HS, and Pan HL (2012a) Switch to glutamate receptor 2-lacking AMPA receptors increases neuronal excitability in hypothalamus and sympathetic drive in hypertension. J Neurosci 32:372-380.
34. Li L, Cao XH, Chen SR, Han HD, Lopez-Berestein G, Sood AK, and Pan HL (2012b) Up-regulation of Cavβ3 subunit in primary sensory neurons increases voltage-activated Ca2+ channel activity and nociceptive input in neuropathic pain. J Biol Chem 287:6002-6013.
35. Lieberman DN and Mody I (1994) Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase. Nature 369:235-239.
36. Lieberman DN and Mody I (1999) Casein kinase-II regulates NMDA channel function in hippocampal neurons. Nat Neurosci 2:125-132.
37. Liu J, Farmer JD, Jr, Lane WS, Friedman J, Weissman I, and Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
38. Miletic G, Pankratz MT, and Miletic V (2002) Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats. Pain 99:493-500.
39. Nelson KA, Park KM, Robinovitz E, Tsigos C, and Max MB (1997) High-dose oral dextromethorphan versus placebo in painful diabetic neuropathy and postherpetic neuralgia. Neurology 48:1212-1218.
40. Pan HL, Khan GM, Alloway KD, and Chen SR (2003) Resiniferatoxin induces paradoxical changes in thermal and mechanical sensitivities in rats: mechanism of action. J Neurosci 23:2911-2919.
41. Pinna LA (1990) Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim Biophys Acta 1054:267-284.
42. Rabben T, Skjelbred P, and Oye I (1999) Prolonged analgesic effect of ketamine, an N-methyl-D-aspartate receptor inhibitor, in patients with chronic pain. J Pharmacol Exp Ther 289:1060-1066.
43. Raman IM, Tong G, and Jahr CE (1996) Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16:415-421.
44. Sacks DB, Davis HW, Williams JP, Sheehan EL, Garcia JG, and McDonald JM (1992) Phosphorylation by casein kinase II alters the biological activity of calmodulin. Biochem J 283:21-24.
45. Sang CN, Booher S, Gilron I, Parada S, and Max MB (2002) Dextromethorphan and memantine in painful diabetic neuropathy and postherpetic neuralgia: efficacy and dose-response trials. Anesthesiology 96:1053-1061.
46. Santos SF, Rebelo S, Derkach VA, and Safronov BV (2007) Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J Physiol 581:241-254.
47. Sarno S, Moro S, Meggio F, Zagotto G, Dal Ben D, Ghisellini P, Battistutta R, Zanotti G, and Pinna LA (2002) Toward the rational design of protein kinase casein kinase-2 inhibitors. Pharmacol Ther 93:159-168.
48. Sarno S, Reddy H, Meggio F, Ruzzene M, Davies SP, Donella-Deana A, Shugar D, and Pinna LA (2001) Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 ('casein kinase-2'). FEBS Lett 496:44-48.
49. Schwartzman RJ, Alexander GM, Grothusen JR, Paylor T, Reichenberger E, and Perreault M (2009) Outpatient intravenous ketamine for the treatment of complex regional pain syndrome: a double-blind placebo controlled study. Pain 147:107-115.
50. Soto D, Pancetti F, Marengo JJ, Sandoval M, Sandoval R, Orrego F, and Wyneken U (2004) Protein kinase CK2 in postsynaptic densities: phosphorylation of PSD-95/SAP90 and NMDA receptor regulation. Biochem Biophys Res Commun 322:542-550.
51. Tong G, Shepherd D, and Jahr CE (1995) Synaptic desensitization of NMDA receptors by calcineurin. Science 267:1510-1512.
52. Wang XL, Zhang HM, Chen SR, and Pan HL (2007) Altered synaptic input and GABAB receptor function in spinal superficial dorsal horn neurons in rats with diabetic neuropathy. J Physiol 579:849-861.
53. Wang YT and Salter MW (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369:233-235.
54. Ye ZY, Li L, Li DP, and Pan HL (2012) Casein kinase 2-mediated synaptic GluN2A up-regulation increases N-methyl-D-aspartate receptor activity and excitability of hypothalamic neurons in hypertension. J Biol Chem 287:17438-17446.
55. Yu XM, Askalan R, Keil GJ, 2nd, and Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.
56. Zhao YL, Chen SR, Chen H, and Pan HL (2012) Chronic opioid potentiates presynaptic but impairs postsynaptic N-methyl-D-aspartic acid receptor activity in spinal cords: implications for opioid hyperalgesia and tolerance. J Biol Chem 287: 25073-25085.
57. Zhou HY, Chen SR, Byun HS, Chen H, Li L, Han HD, Lopez-Berestein G, Sood AK, and Pan HL (2012) N-methyl-D-aspartate receptor- and calpain-mediated proteolytic cleavage of K+-Cl-cotransporter-2 impairs spinal chloride homeostasis in neuropathic pain. J Biol Chem 287:33853-33864.
58. Zhou HY, Chen SR, Chen H, and Pan HL (2008) Sustained inhibition of neurotransmitter release from nontransient receptor potential vanilloid type 1-expressing primary afferents by mu-opioid receptor activation-enkephalin in the spinal cord. J Pharmacol Exp Ther 327:375-382.
59. Zhou HY, Chen SR, Chen H, and Pan HL (2010) Opioid-induced long-term potentiation in the spinal cord is a presynaptic event. J Neurosci 30:4460-4466.
60. Zhou HY, Chen SR, Chen H, and Pan HL (2011a) Functional plasticity of group II metabotropic glutamate receptors in regulating spinal excitatory and inhibitory synaptic input in neuropathic pain. J Pharmacol Exp Ther 336:254-264.
61. Zhou HY, Chen SR, and Pan HL (2011b) Targeting N-methyl-D-aspartate receptors for treatment of neuropathic pain. Expert Rev Clin Pharmacol 4:379-388.